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Echinoid Metamorphosis: Retraction and Resorption of Larval Tissues

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Echinoid Metamorphosis: Retraction and Resorption of Larval Tissues International Echinoderms Conference, Tampa Bay. J.M.Lawrence, ed. (A.A.Balkema, Rotterdam, 1982) Echinoid metamorphosis: retraction and resorption of larval tissues ROBERT D.BURKE University of Victoria, Canada 1 ABSTRACT Highsmith, 1977). It is not certain how larvae perceive these cues, though sensory During the first fifteen minutes of meta- receptors have been identified which may morphosis in Arbacia punctulata and be involved in the perception of tactile Dendraster excentricus, larval tissues are components (Burke, 1980). There are several retracted and resorbed into the aboral accounts of the fates of larval and adult surface of the juvenile. Ultrastructural tissues at metamorphosis (MacBride, 1903; observations of the sequence indicate that Chia and Burke, 1978) and several of the there is an immediate contraction of the developmental processes of metamorphosis epidermis mediated by actin-like filaments. have been identified (Cameron and Hine- Within five minutes, the epidermis begins gardner, 1978; Chia and Burke, 1978). to histolysize and undergoes necrosis. The purpose of this report is to present Metamorphosis can be induced by brief, preliminary findings of studies of echinoid electrical stimulation of either of two metamorphosis in which the main objectives regions of neuropile. Catecholamine neuro- are to characterize developmental processes transmitters will initiate the contraction- of metamorphosis and determine how these histolysis-necrosis sequence in isolated processes are initiated and controlled. larval arms. Treatment with the ionophores This paper describes the sequence of devel- A23187 or X537A will induce only contrac- opmental events that take place in the tion, whereas histolysis without contrac- larval arms during metamorphosis. The arms tion can be induced by treatment with an are specialized larval structures which extract of histolysizing larval tissues. degenerate during metamorphosis. Results It is proposed that the nervous system are presented that suggest the retraction controls initiation of the retraction and and resorption of larval tissues may be resorption sequence during echinoid meta- controlled in part by the larval nervous morphosis. system. 2 INTRODUCTION 3 MATERIALS AND METHODS It has been reported for several species of All larvae were cultured using the standard echinoids that certain environmental cues procedures outlined by Hinegardner (1969) will stimulate competent larvae to metamor- and Strathmann (1968). Adult Dendraster phose (Strathmann, 1978 for review). excentricus were collected intertidally at Presumably, the environmental cues act as Sidney Island, B.C. Canada, and adult stimuli for receptors on the larva. The Arbacia punctulata were collected sub- receptors, in turn, communicate with the tidally at St. Lucie Inlet, Fla. USA. tissues that are the effectors of metamor- Larvae were prepared for transmission phosis. The developmental processes that electron microscopy (TEM) by initially transform or activate these tissues are the fixing in a solution containing 2.5% glutar- response, metamorphosis. Evidence for such aldehyde, 0.2 M phosphate buffer, and 0.14 M a hypothesized stimulus-response mechanism NaCl. Specimens were post-fixed for 1 hr is not complete. Environmental cues have at room temperature in 2% osmium tetroxide been demonstrated but not fully character- in 1.25* sodium bicarbonate. Dehydration ized (Cameron and Hinegardner, 1974; was by alcohol exchange and specimens were 513 infiltrated and embedded in Epon. Sections skeletal rod piercing the ti] of the arm were stained with 50"; ethanol saturated and the tube of epidermis collapsing and with uranyl acetate and lead hydroxide folding as it is drawn towards the base of chelated with sodium citrate. Observations the arm. Th^ skeletal rod is eventually and micrographs were m .de using a Zeiss EM dropped from the aboral surface of the 9S-2. j uvcnile. Eor experiments with the ionophores The structural changes accompanying the A23187 and X537A (courtesy of W.E. Scott, retraction of the larval arms are first Hoffman-LaRoche Ltd.), and neurotransmitter apparent in tissues fixed thirty seconds substances, individual larval arms were after retraction begins. Bundles of micro- dissected from competent larvae with fine filaments (5 to 7 nm in diameter) which are tungsten needles and placed in test solu- not apparent in competent larvae occur in tions in depression slides or small watch the cvtoplasm of cells of the epidermis and glasses. The ionophores are not readily the ciliary bandr (Fig. 2). In the epi- soluable in sea water, so dimethyl sulf- dermal cells, the microfilarnent bundles oxide (DMSO) was used to nr»-pare stock occur throughout the cytoplasm and seem most solutions. Final test solutions contained numerous in the cells adjacent to the 2" DMSO. To test the effects of electrical ciliary bands (Fig. 3). The filaments are stimulation, competent larvae were attached usually oriented along the long axis of the to a fine tipped, polyethylene suction arm. Filaments within the ciliary bands electrode (tip diameter 40-60 ].im) and occur in both apical and basal portions of stimulated with either a D.C. square wave the ciliated cells. In the apical regions stimulator or a regulated D.C. source. of the ciliated cells the filaments are oriented at right angle to the long axis of the arm (Fig. 5), whereas in the basal 4 RESULTS portions of the cell the filaments are oriented along the long axis of the cells. 4. 1 rval arms In larvae fixed two minutes after the beginning of arm r^^act ion, the epidermis Competent echinoplutei have eight larval is pleated and folded as the arm contracts, arms which in the case of Arbacia punctu- and the ciliary bands fold inwards toward lata may be up to 800 um long. The arms the center of the arm. Filament bundles are outlined by a dense band of cilia and arc more numerous in the cells of the epi- function as locomotory and feeding organs dermis than a ter 30 seconds and are also throughout the life of the larva. In apparent within the mesenchymal cells Arbacia punctulata the arms are circular associated with the skeletal rod (Fig. 4). in cross section (Fig. It). The exterior The c_i 1 iary bands become disorganized as surface of the arm is comprised o: squarn- they to^d inward, fch6 cells detach and ous epithelium 1 to 2 pm thick and the begin 'o round ip (Fig. lb). Within the surface of the arm directec towards the cytoplusm of the eiHated cells axonemes larval mouth is columnar epithelium 4 urn and fibrils of cllii may be found (Fig. 6). thick. The ciliary bands are thickenings After five minutes the arms have retracted of the epidermis that are elliptical in to about one nuartor nf their original cross section and are comprised of spindle length. The , irms a^e now a thin cuboidal shaped cells each of which has a single epithelium surrroundi :ig a core of loosely cilium at its apical surface. A sinqLe associated individual cells (Fig. lc). The tract of axons, 1 to 2 urn in diameter lies c 11s within the core are the cells of the in a central position embedded in the base ciliary bands, tie axonal tracts, and the of the ciliary band. Each arm is supported mesenchyme. Fi_l aments can sti: 1 be observe^, by a single skeletal rod which is located within the covering epithelium and some of in the central space of the arms and has the cells within the core. However, ciliarv associated with it numerous mesencxymal band cells in the core of the retracted arms are rnnnded-up, have lost their apical-basal Metamorphosis begins with the eversion p^lirity, and have nuclei that are more of an aoulc rudiment from an inpoc'-:et ing granular and electron dense than at previous on the left side of the larva (see iiyman, stages (Fig. 7). Cytoplasmis debris is 1955 for review). The aversion is usually scattered throughout the core of the arms, completed in about 3 to 5 minutes. Begin- and the cells can be seen to have frag- ning at the same time as the eversion, the mented . larval cirrus are retracted into what will After ten minutes the larVal arms have become the abora1 surface of the juvenile. retracted to small knobs on the aboral sur- The retraction r icuires about 20 minutes iace. The cuboidal epithelium covering the to be completed. It begins with the arms has fewer filaments than at previous 514 Fig. 1. Licjht micrographs of cross sections of ] irval arms of7 Arbacia "mnctulata a) prior to metamorphosis, b) two minutes af tei the beuirning o" arm re; L'jrtio , c) Live minutes after the beginning of arm retraction. Kir - 1:) IJRI. Fig. 2. Transmission electron micrograph o:: epithelial cell of larval riri of Arbacia punctulata fixed thirty seconds a:tor t he ben^ning of arm rptraction Arrows indicate f iJ ,:m^nts. Bar - 0.5 um. Fig. 3. Longitudinal section through cells adjacent to the ciliary band in larval arm of Arbacia punctulata fixed thirty seconds after the beginning of arm retraction. Arrows indicate filaments. Bar - 0.5 pm. Fig. 4. Longitudinal section through portion of mesenchymal cel.l associated with larval skeleton in arm of Arbacia punctjL.ta fixed two minutes a:Lor the beginning o! arm retraction. Arrows indicate filaments. Bar - 0,5 \m. Fig. 5. Cross section of larval arm showing apical region of ciliated cells of ciliary band two minutes after the beginning of arm retraction. Arrows indicate filaments. Bar - 0.5 wm. Fig. 6. Basal region of ciliated cells of the ciliary band of larval arm of Arbacia punctulata fixed two minutes after the beginning of arm retraction. Note axonome and fibrils of retracted cilium. Bar - 0.5 pro. Fig. 7. Core region of retracted arm ten minutes after the beginning of arm retraction. Bar - 1 pm. Fig.
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